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Shifts in cranial integration associated with ecological specialization in pinnipeds (Mammalia, Carnivora).

ABSTRACT: Patterns of trait integration reflect the underlying genetic and developmental architecture of morphology and significantly influence the direction of evolution. Nevertheless, the relationship between integration and disparity is complex and unlikely to be uniform across large phylogenetic and ecological scales. To date, there are little data comparing patterns of integration across major ecological transitions, limiting understanding of the processes driving changes in trait integration and their consequences. Here, we investigated patterns of cranial integration and disparity across pinnipeds, three closely related carnivoran families that have undergone a secondary adaptation to the aquatic niche with varying levels of ecological differentiation. With a three-dimensional geometric morphometric dataset of 677 specimens spanning 15 species, we compared five models of trait integration, and examined the effects of sexual dimorphism and allometry on model support. Pinnipeds varied greatly in patterns of cranial integration compared to terrestrial carnivorans. Interestingly, this variation is concentrated in phocids, which may reflect the broader range of ecological and life-history specializations across phocid species, and greater independence from the terrestrial habitat observed in that group, relative to otariids. Overall, these results indicate that major ecological transitions, and presumably large changes in selection pressures, may drive changes in phenotypic trait integration.

SUBMITTER: Randau M

PROVIDER: S-EPMC6458409 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Shifts in cranial integration associated with ecological specialization in pinnipeds (Mammalia, Carnivora).

Randau Marcela M Sanfelice Daniela D Goswami Anjali A

Royal Society open science 20190327 3

Patterns of trait integration reflect the underlying genetic and developmental architecture of morphology and significantly influence the direction of evolution. Nevertheless, the relationship between integration and disparity is complex and unlikely to be uniform across large phylogenetic and ecological scales. To date, there are little data comparing patterns of integration across major ecological transitions, limiting understanding of the processes driving changes in trait integration and the ...[more]

PMID: 31032062

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Project description:BackgroundPhylogenetic comparative methods are often improved by complete phylogenies with meaningful branch lengths (e.g., divergence dates). This study presents a dated molecular supertree for all 34 world pinniped species derived from a weighted matrix representation with parsimony (MRP) supertree analysis of 50 gene trees, each determined under a maximum likelihood (ML) framework. Divergence times were determined by mapping the same sequence data (plus two additional genes) on to the supertree topology and calibrating the ML branch lengths against a range of fossil calibrations. We assessed the sensitivity of our supertree topology in two ways: 1) a second supertree with all mtDNA genes combined into a single source tree, and 2) likelihood-based supermatrix analyses. Divergence dates were also calculated using a Bayesian relaxed molecular clock with rate autocorrelation to test the sensitivity of our supertree results further.ResultsThe resulting phylogenies all agreed broadly with recent molecular studies, in particular supporting the monophyly of Phocidae, Otariidae, and the two phocid subfamilies, as well as an Odobenidae + Otariidae sister relationship; areas of disagreement were limited to four more poorly supported regions. Neither the supertree nor supermatrix analyses supported the monophyly of the two traditional otariid subfamilies, supporting suggestions for the need for taxonomic revision in this group. Phocid relationships were similar to other recent studies and deeper branches were generally well-resolved. Halichoerus grypus was nested within a paraphyletic Pusa, although relationships within Phocina tend to be poorly supported. Divergence date estimates for the supertree were in good agreement with other studies and the available fossil record; however, the Bayesian relaxed molecular clock divergence date estimates were significantly older.ConclusionOur results join other recent studies and highlight the need for a re-evaluation of pinniped taxonomy, especially as regards the subfamilial classification of otariids and the generic nomenclature of Phocina. Even with the recent publication of new sequence data, the available genetic sequence information for several species, particularly those in Arctocephalus, remains very limited, especially for nuclear markers. However, resolution of parts of the tree will probably remain difficult, even with additional data, due to apparent rapid radiations. Our study addresses the lack of a recent pinniped phylogeny that includes all species and robust divergence dates for all nodes, and will therefore prove indispensable to comparative and macroevolutionary studies of this group of carnivores.

Project description:BackgroundAlthough variation provides the raw material for natural selection and evolution, few empirical data exist about the factors controlling morphological variation. Because developmental constraints on variation are expected to act by influencing trait correlations, studies of modularity offer promising approaches that quantify and summarize patterns of trait relationships. Modules, highly-correlated and semi-autonomous sets of traits, are observed at many levels of biological organization, from genes to colonies. The evolutionary significance of modularity is considerable, with potential effects including constraining the variation of individual traits, circumventing pleiotropy and canalization, and facilitating the transformation of functional structures. Despite these important consequences, there has been little empirical study of how modularity influences morphological evolution on a macroevolutionary scale. Here, we conduct the first morphometric analysis of modularity and disparity in two clades of placental mammals, Primates and Carnivora, and test if trait integration within modules constrains or facilitates morphological evolution.Principal findingsWe used both randomization methods and direct comparisons of landmark variance to compare disparity in the six cranial modules identified in previous studies. The cranial base, a highly-integrated module, showed significantly low disparity in Primates and low landmark variance in both Primates and Carnivora. The vault, zygomatic-pterygoid and orbit modules, characterized by low trait integration, displayed significantly high disparity within Carnivora. 14 of 24 results from analyses of disparity show no significant relationship between module integration and morphological disparity. Of the ten significant or marginally significant results, eight support the hypothesis that integration within modules constrains morphological evolution in the placental skull. Only the molar module, a highly-integrated and functionally important module, showed significantly high disparity in Carnivora, in support of the facilitation hypothesis.ConclusionsThis analysis of within-module disparity suggested that strong integration of traits had little influence on morphological evolution over large time scales. However, where significant results were found, the primary effect of strong integration of traits was to constrain morphological variation. Thus, within Primates and Carnivora, there was some support for the hypothesis that integration of traits within cranial modules limits morphological evolution, presumably by limiting the variation of individual traits.

Project description:Ursidae is a monophyletic group comprised of three subfamilies: Tremarctinae, Ursinae and Ailuropodinae, all of which have a rich geographical distribution. The phylogenetic relationships within the Ursidae group have been underexamined, especially regarding morphological traits such as the basicranium. Importantly, the basicranium is a highly complex region that covers a small portion of the skull, combining both structural and functional aspects that determine its morphology. Phylogenetic hypotheses of the Ursidae (including Tremarctinae) have been made based on morphological characters that considers skull, mandible and teeth features, while specific characters of the auditory region and basicranium have not been taken into account. To do this, we analyse the shape and size macroevolution of the basicranium of Ursidae, testing its morphological disparity in a phylogenetic context, which is quantified by means of the phylogenetic signal. We investigated phylogenetical autocorrelation by shape (depicted by Principal Components Analysis scores from previous published analyses) and basicranium size (depicted by centroid size, CS) using an orthonormal decomposition analysis and Abouheif C mean. The main advantages of these methods are that they rely exclusively on cladogram topology and do not require branch-length estimates. Also, an optimisation of the ancestral nodes was performed using TNT 1.5 software. In relation to the phylogenetic signal, both methods showed similar results: the presence of autocorrelation was detected in PC1 and PC2, while in PC3, PC4 and PC5 and in the size of the basicranium (CS), the absence of autocorrelation occurred. The most significant nodes (where there is autocorrelation) are the basal nodes 'Ursidae' and 'Ursinae-Tremarctinae'. Within this last group, distinctive basicranium morphology is observed, being more conservative in Tremarctinae than in Ursinae. The differences between these subfamilies could be related to historical events involving varying food and environmental preferences. The high phylogenetic signal in the node Tremarctinae probably indicates that the basicranium configuration of these bears was obtained early in their evolutionary history. Finally, our results of the basicranium and skull length ratios indicate that in Tremarctinae, the basicranium size was not determined by phylogeny but instead by other factors, such as adaptive responses to climatic changes and competition with other carnivores.

Dataset Information

Shifts in cranial integration associated with ecological specialization in pinnipeds (Mammalia, Carnivora).

Publications

Shifts in cranial integration associated with ecological specialization in pinnipeds (Mammalia, Carnivora).

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